Change In Feeding Rate Research Articles

Daily feeding rates in herbivorous labroid fishes

Estimates of daily feeding rates were obtained for two groups of herbivorous labroid fishes, one confined to cold water and the other to tropical reef environments. These were the family Odacidae, represented by Odax pullus from New Zealand waters, (Goat Island Bay: Latitude 36° South; on the northeastern coast of New Zealand) and the family Scaridae, represented by Scarus rivulatus, S. schlegeli and S. sordidus from the northern Great Barrier Reef (Lizard Island; a mid-shelf reef at 14° South latitude). Observations on the odacid were made in 1984 and in 1992, and on the scarids in 1984 and 1988. O. pullus displayed a diurnal feeding pattern in which the rates (expressed as bites min-1) are greatest early in the day. The mean combined feeding rate for three size groups (juveniles, subadults and adults) peaked (average of 2.9 bites) from 06.00 to 08.00 hrs and declined fourfold to a combined average of 0.7 bites min-1 by midday. The greatest mean feeding rate recorded was 3.7 bites min-1, with an overall mean of 1.8 bites min-1. For subadults and adults there were consistent trends in feeding, with subadults feeding at a greater rate than adults and both groups displaying a decline in feeding rate during the day. The change in feeding rate with time of day was statistically significant in both groups. The pattern for juvenile O. pullus was different from that in the two larger size groups in that juveniles did not show a uniform decline in feeding with time of day. For scarids, the daily feeding rate varied by site, but the pattern was similar for all species, characterised by initial low rates increasing to higher but variable levels by midday. The influence of both site of feeding and time of day on feeding rate was confirmed by analysis. The overall mean values for each species were 20.1 bites min-1 for S. rivulatus, 19.7 bites min-1 for S. schlegeli and 14.9 bites min-1 for S. sordidus. For scarids, the peak feeding rates varied from 19.3 to 32.8 bites min-1, with overall rates from 14.9 to 21.1 bites min-1. Estimates of activity and movement patterns during feeding were obtained for O. pullus. Distance moved per unit time was highly variable, 0.1 to 47.5 m min-1, with a mean of 8.5 m min-1 (SD=9.9). Trends in movement among sexes and size classes were obscured by the variable movement patterns of individual fishes.

Retention of intragastric transmitters after voluntary ingestion by captive cod, Gadus morhua L.

Squid‐encapsulated acoustic transmitters were ingested by Atlantic cod, Gadus morhua, (3128–10 221 g) held in captivity at 12° C. Retention times ranged from 5 to > 21 days. There was no significant change in feeding rate after transmitter ingestion.

Evaluation of Predator‐Induced Stress on Field Populations of Stoneflies (Plecoptera)

The influence of predaceous fish in affecting components of fitness of immature and adult macroinvertebrates was examined using a predator enclosure/exclosure experiment in a southern Ontario stream. The stonefly Paragnetina media is a semivoltine species with a midsummer emergence period. After exposure of P. media to rainbow trout (Oncorhynchus mykiss) between May and August (repeated twice, 1987 and 1989), we observed significant reductions in nymphal density, size (head width), and conditions (mass/head width). Reductions in density were attributable to nymphal emigration and predation. Selective predation on larger stoneflies (direct effects), together with changes in nymphal feeding rate, activity, and distribution (indirect effects), reduced size and condition of stoneflies exposed to trout. After August—to—October (1986 and 1989) and January—to—April (1988) exposures, we observed no effect of trout on these parameters. Adults stoneflies (P. media and Alloperla mediana) cannot feed, and consequently any energy that they channel into reproductive efforts must be derived from the aquatic stage. Thus, we postulated that the impact of trout on immature P. media and A. mediana might manifest itself negatively on stonefly adults. Although size and emergence pattern of adult P. media and A. mediana did not differ between enclosure/exclosure sections of stream, in the presence of trout both species suffered significant reductions in condition, fecundity, and total number to emerge. These findings demonstrate that direct and indirect effects of a predator can cascade from immature to adult prey and from aquatic to terrestrial ecosystems.

Foraging Phenology of the Formosan Subterranean Termite (Isoptera: Rhinotermitidae) in Louisiana

-A 2-yr field study was done to measure seasonal changes in feeding rates, number of workers, mass of individual workers and percentage of soldiers of foraging groups from colonies of the Formosan subterranean termite, Coptotermes formosanus Shiraki, living in cypress trees (Taxodium distichum [L.] Rich.) at the Calcasieu River near Lake Charles, Louisiana. There was distinct seasonality with most dependent variables. Feeding rate was highest in summer and varied positively with day length and daily maximum temperature. Number of workers was highest in summer, increased with increasing day length but leveled off at higher values of day length. Mass of individual workers was fairly uniform but tended to be higher in summer; it varied positively with temperature but leveled off at higher temperatures. Percentage of soldiers was highest in early winter and varied inversely with day length and temperature. On average, these colonies ate 7265.2 ? 1653.3 g (range = 4647.1 g to 9969.9 g) of pine (Pinus sp.) wood in baits over 2 yr.

The Effects of Sewage Sludge On Two Life-History Stages of Mytilus Edulis

Abstract Adult and embryos of the common mussel 'Mytilus edulis were exposed to dilutions of, respectively, whole and seawater-extracted sewage sludge. the response of adult mussels was measured as change in feeding and respiration rate after four weeks' continuous exposure, while embryo response was assessed as the percentage of normal, D-shaped larvae after 24 hours, exposure. Adult feeding rate was significantly depressed, and respiration rate significantly increased, at the lowest sludge concentration used (0.02%), and the effect appeared to be attributable to the dissolved rather than to the participate phase of the test medium. the developmental EC50 for embryos was estimated to be 0.15% sewage sludge. at dilutions of 1:600 to 1:5000, therefore, the sewage sludge investigated contained unidentified desorbable components toxic to planktonic and benthic life-history stages of a common marine invertebrate. Aerial application of fenthion, 0.0-dimethyl 0-[3-methyl-4-(methylthio)phenyl] phosphorothioate, is widely used to control adult mosquito populations in the Florida coastal marshes. Although not sprayed on water intentionally, aerial spray may accidentally drift into estuarine, coastal and offshore waters. Laboratory and field studies were previously conducted to determine the assimilation capacity of fenthion in coastal water and its effects on non-target organisms. Fenthion, once deposited to the coastal water, normally undergoes chemical, photochemical and biological processes. the effect of pH, salinity, natural sunlight and biological activities in the coastal water are discussed. the half-life of fenthion in the offshore, inlet coastal water, estuarine and mangrove swamp waters were found to be 21.1, 5.6, 4.2 and 2.9 days, respectively. in natural conditions, photolysis and biological activities are the two dominant pathways for assimilating fenthion in the water. Four aerial field studies were also conducted to investigate the deposition rate of fenthion in the water. the deposition rate of fenthion aerial spray into the coastal water and its acute toxicity on non-target estuarine organisms were determined. After each spray, fenthion concentration was normally increased and peaked at 45 minutes and then gradually decreased. After 24 hours, only a trace of fenthion (0.01 μgL−1 ) was detected. Animal toxicity tests conducted in the field included adults of the calanoid copepod, Acartia tonsa, eggs and juveniles of three species of fishes. Statistically, significant mortality occurred only for copepods in one of the four tests. Water quality such as temperature could play an important role in the sensitivity of copepods to the fenthion.

Seasonal changes in feeding rate, digestive enzyme activity, and assimilation efficiency of Calanus pacificus

Seasonal changes in feeding rate, digestive enzyme activity, and assimilation efficiency of Calanus pacificus

Formation of Annuli in Otoliths of Bluegills

Abstract Hatchery-spawned bluegills Lepomis macrochirus were reared in controlled laboratory conditions to evaluate the effects of water temperature, photoperiod, and feeding rates on opaque and translucent band formation in otoliths. Opaque bands were associated with periods of slow growth, and translucent bands were associated with periods of fast growth. Marginal increments (translucent bands distal to opaque bands) formed at 22°C or higher water temperatures. Although opaque bands formed, no marginal increments formed when water temperature was below 22°C. Fish exposed to a cycle of warm water (≥22°C), cool water (<17°C), and warm water formed a second opaque band and marginal increment. Opaque bands and marginal increments formed in bluegill otoliths at similar temperatures in outdoor tanks, in two lakes, and in the laboratory. Opaque bands also were induced by changes in photoperiod and feeding rate; however, the effects of photoperiod and feeding rate were inconsistent, and the opaque bands formed ...

Ontogenetic Habitat Shifts in Bluegill: The Foraging Rate‐Predation Risk Trade‐off

The bluegill sunfish (Lepomis macrochirus) undergoes several habitat shifts between the littoral and pelagic zones of small lakes during its life history. After hatching in the littoral zone, bluegill fry migrate to the pelagic zone to feed on zooplankton. In this study the fry then returned to the littoral zone in four different lakes at a relatively constant size of °12.5 mm standard length. Several years are spent feeding in the littoral zone vegetation before the bluegill again shifts to feeding on zooplankton, first in the water column above littoral vegetation and subsequently in the true pelagic zone. This shift to feeding on zooplankton occurred at a specific body size within a lake, but the size ranged from 50 to 83 mm among five different lakes. The size at which the shift occurred was directly correlated with the density of the major predator of the bluegill in these lakes, the largemouth bass (Micropterus salmoides). We demonstrate that the bluegill is faced with a growth (or feeding) rate—predation risk trade—off in making these habitat shifts. Analysis of stomach contents, the growth of small fish caged in the pelagic zone, and predictions of foraging rates in both habitats all indicate that the pelagic zone is the more profitable habitat for all size classes of the bluegill. Through a series of pond experiments we further show that risk of predation by largemouth bass was 40—80 times as great for small bluegills in the open water as for those in the vegetation. We interpret the patterns of habitat use by the bluegill in terms of a model that explicitly weights the costs (predation) and benefits (growth) of making a size—specific habitat shift to the pelagic. Finally, we discussed evidence that the bluegill can facultatively respond to changes in feeding rates and predation risk, and the consequences of such ontogenetic habitat shifts to community dynamics.

Feeding and Digestion in Suspension-Feeding Bivalve Molluscs: The Relevance of Physiological Compensations

SYNOPSIS. Intertidal suspension-feeding bivalves face reductions in the time available for feeding proportional to the duration of aerial exposure. Such individuals do not compensate by increasing their rates of feeding during immersion. Simulations of feeding behaviour, in terms of the energetic balance between the costs and the gains of changes in feeding rate, suggest that variation from the rates characteristic of the sublittoral condition would not enhance net energy gain for intertidal individuals. These findings are consistent with evidence of potential food limitation in the natural sublittoral habitat. Nevertheless, hydrodynamic factors may enhance the supply of food on the shore, so ameliorating the disadvantages of reduced feeding time. In addition, potential physiological compensations for reduced dietary quality include changes in gut residence time, the volume of gut occupied for digestion and (possibly) also in the provision of appropriate digestive enzymes. However, these compensations require days or weeks and are inappropriate on tidal time scales.

Gut Fullness of the Deposit-Feeding Amphipod, Pontoporeia hoyi, in Southeastern Lake Michigan

Pontoporeia hoyi Smith, a deposit-feeding amphipod and a prominent member of the Great Lakes macrobenthic community, was collected at a 45-m-deep site in southeast Lake Michigan during October 1983 and March, May, June, August, and September 1984. Substantial numbers of animals with empty or partially-full guts indicated that P. hoyi feeds intermittently, unlike other continuous-feeding amphipods which routinely maintain uniformly full guts among all members of a population. The incidence of animals with empty, partially-full, and full guts also varied significantly with animal size and sampling date and implied that aspects of the amphipod's life history, and seasonality, were primarily responsible for changes in feeding rates. Overall, P. hoyi gut fullness was greatest in spring and, secondarily, in autumn, reflecting an opportunistic feeding strategy that exploited newly-deposited detritus generated from spring and autumn phytoplankton blooms. This strategy, in association with P. hoyi's known capacity to store energy as lipids may largely explain P. hoyi's exclusive and widespread distribution in profundal areas of the upper Great Lakes, compared to other amphipods.

Parental Care in the Wheatear Oenanthe oenanthe: Effects of Nestling Age and Brood Size

Changes in different aspects of parental care of Wheatears with nestling age and brood size were studied over 4 yr in two Swedish breeding populations. Some broods were enlarged or reduced to increase the range of observed brood sizes. The proportion of time females spent brooding decreased with nestling age until day 8, but the mean duration of brooding bouts did not, implying that females reduced the frequency of brooding bouts as homeothermic capacity of the young improved. Females reduced mean bout duration with brood size but not the total time spent brooding. The different effects of nestling age and brood size, and the negative effect of females' feeding rates on brooding commitment suggest that the food requirements of the young may affect female brooding behaviour independently of the homeothermic capacity of the young. Feeding rates of males and females increased similarly throughout the nestling period and reached a plateau from day 9 to fledging at about day 14. Load size and prey size increased with nestling age, and the proportions of spiders and small caterpillars in the diet of nestlings decreased. Males delivered larger loads than females. The relationship between feeding rates and brood size during the plateau phase differed depending on whether manipulated broods were included in the analysis or not. For unmanipulated broods, feeding rates did not increase with brood size and there was thus a decrease in feeding rates per nestling with brood size. When including manipulated broods in the analysis, there was a decelerating positive relationship of feeding rates with brood size. When removing the small broods, no decrease in feeding rates per nestling with brood size was found in the joint analysis of all broods. Brood manipulations led to changes in feeding rates with respect to the normal pattern observed. Future studies of parental care should consider these effects of manipulations before deriving any definitive conclusion about brood size effects.

Gut-marker and gut-fullness methods for estimating field and laboratory effects of sediment transport on ingestion rates of deposit-feeders

By developing a method for quantifying feeding rate in the presence of sediment transport, we determined whether sediment transport or one of its correlates influenced feeding rate of deposit-feeders in the field. The method entailed application and subsequent removal of magnet-susceptible marker particles, so that no marker was present in the ambient sediments during the period over which feeding rate actually was measured. Error variance was reduced by a paired statistical design in which the technique was used twice in the same individuals, to assess feeding rate immediately prior to the sediment transport event as well as during it. Low levels of sediment transport significantly affected feeding rates of Pseudopolydora kempi japonica Imajima & Hartman (a spionid polychaete) both in a small, imprecise, laboratory flume and in an intertidal environment characterized from late spring through early fall by a short pulse of sediment transport coincident with the incoming tide. Deposit-feeding rates immediately after the latter pulse were enhanced by a (geometric) mean of 50% in field trials from May through October. Both in the laboratory and in the field, however, the magnitude of the (albeit statistically significant) sediment transport effect was overshadowed by variation due to nutritional history of individuals and to other unidentified factors. The form of the field data for P. kempi japonica (feeding rates estimated for two successive intervals in the same individuals) allowed us, in addition, to analyze the response of gut fullness to mean feeding rate (averaged over the two feeding bouts), previous feeding rate (first bout), most recent feeding rate (second bout) or recent change in feeding rate (difference between first and second bouts). The strongest correlation was found with the last of these variables, suggesting that gut fullness may provide a tracer-free method of gaining some kinetic information on continuously feeding animals. Contrary to prevailing impressions, gut fullness in such continous feeders may provide more information on recent change in feeding rate than on feeding rate itself. We gathered additional data on P. kempi japonica that differed in emersion history (in tide-pools versus outside them prior to the pulse of sediment transport with the incoming tide) but were not exposed to markers. Animals both inside and outside tide-pools showed fuller guts immediately after the sediment transport pulse, consistent with an interpretation of accelerated feeding caused by some aspect of the sediment transport event. Incidentally collected individuals of Hobsonia florida (Hartman) (an intertidal ampharetid polychaete), on the other hand, showed no obvious response to the same conditions that triggered accelerated feeding and fuller guts in Pseudopolydora kempi japonica.

Changes in Scanning and Feeding Rates with Group Size among American Goldfinches

Changes in Scanning and Feeding Rates with Group Size among American Goldfinches

Enzymatic adaptations of herbivorous insects and mites to phytochemicals

A variety of oxidases, reductases, esterases, epoxide hydrolases, and group transferases in herbivorous insects and mites detoxify and facilitate the excretion of toxic phytochemicals (allelochemicals). Current theory indicates that the cytochrome P-450-dependent mixed-function oxidases (MFOs) are by far the most important enzymes because they have many attributes that are essential for an effective detoxification system. Data presented here on the midgut microsomal MFO activity of larvae of the gypsy moth,Lymantria dispar, are discussed in the light of previous work and support the theory. In the gypsy moth, the MFO levels exhibit a parallel trend with changes in specific feeding rates, and changes in the specific activity of the enzyme appear to be regulated ontogenetically and by inductive effect of chemicals in the diet. The specific activity of the MFOs rises more sharply on leaves of a highly preferred type-1 plant, the pin oak, than on an artificial wheat germ diet; the increase from mid-second instar to mid-fifth is 4.5- and 1.8-fold, respectively. The relationship of food consumption rate to increase in body mass (W) was slightly in excess of a 1∶1 ratio for both pin oak and the artificial diet, indicating that the feeding rate surpasses the increase in W (a rare phenomenon in insects). Moreover, the surface-to-volume ratios are fairly constant for combined data of gut lumen and epithelium in second to fifth instars, because the volume occupied by the epithelial cells is much larger than in older ones. Thus, it is concluded that greater specific activity of the MFO is necessary with larval advancement to higher instars in order that they may process dietary allelochemicals with an efficiency comparable to younger larvae. Additional data suggest that MFO level increases reflect further adaptation to: (1) normal, seasonal changes in plants' allelochemical composition and concentration; (2) increase in allelochemical concentration in response to leaf damage; and (3) the risk faced by dispersing larvae of encountering a greater amount and variety of allelochemicals on suboptimal/ less suitable plants. Evidence also has emerged recently for MFO-catalyzed metabolism/deactivation of numerous plant allelochemicals, including compounds that induce the enzyme. MFOs are further adapted for participation in the biogenesis of substances physiologically important to insects. Moreover, the catalytic center of the MFO system, cytochrome P-450, occurs in multiple forms; the significance of this important feature is discussed.

Time budgets in growing chicks

The manner in which rapidly growing chicks distribute their time among diurnal activities was measured in two studies in which the amount of available light was varied to match seasonal extremes. The effectiveness of the chick's time budgets was assessed in terms of the impact on growth. In Experiment 1, 24-hr patterns of feeding, drinking, nesting, and wheel-running were recorded during successive photoperiods with 12, 6, 18, and 12 hr of light when access to a social partner was concurrently available. In Experiment 2, access to a social partner was an exclusive activity. In both studies, chicks' 24-hr behavioral patterns in response to temporal constraints on their diurnal activities were surprisingly plastic, permitting them to defend a normal and high rate of growth. This was accomplished by changes in feeding rate and by nocturnal feeding rather than by systematic elimination of other diurnal activities. When sociality and feeding were competing activities, feeding time decreased and feeding rate increased such that contact with a conspecific as well as rapid growth were defended. The absolute amount of time spent in measured activities was invariant within subjects irrespective of age, photoperiod, or the number and type of activities recorded, providing evidence of time budgets in immature organisms. In both studies, buffer time (the amount of time spent in no activity) emerged as a significant aspect of the daily time budget that is defended through a variety of enviromental challenges.

Water Flux and Water Requirement in Free-living Antelope Ground Squirrels Ammospermophilus leucurus

Seasonal changes in H₂O flux rates (H³HO) were determined in free-living antelope ground squirrels (Ammospermophilus leucurus) in the Mojave Desert. Itemized H₂O budgets were obtained for ground squirrels in the laboratory eating natural vegetation, seeds, and arthropods. Ground squirrels obtained excess H₂O while eating succulent annual plants in the spring and arthropods. When provided with seeds and minimum H₂O they decreased their evaporative H₂O loss and reduced urine and fecal H₂O content. Changes in feeding rate, assimilation efficiency, or metabolic rate were unimportant in reducing H₂O loss. In the field, H₂O influx decreased from 238 ml $kg^{-1}$ $day^{-1}$ in the early spring to 85 ml $kg^{-1}$ $day^{-1}$ in the late fall and winter. This decrease paralleled a decrease in the H₂O contents of the plants the ground squirrels consumed. The minimum H₂O requirement of free-living ground squirrels was expressed as required minimum food H₂O content. Leaves must be > 45% H₂O to supplement an otherwise ...

Pathophysiological influences of the Heterorhabditis bacteriophora complex on fifth-instar larvae of the red humped caterpillar, Schizura concinna: Changes in feeding rate, larval weight, and frass production

At 28.5°C, oral dosages of the invasive juveniles of Heterorhabditis bacteriophora and intrahemocoelic injections of its associated bacterium, Xenorhabdus luminescens, resulted in a decrease in larval feeding rate, larval wet weight, and frass production in its host, the seventh-instar larvae of Schizura concinna.

Feeding rates of planktonic copepods from a tropical sea

The feeding rates of the marine planktonic copepods, Eucalanus subcrassus Giesbrecht, Tortanus gracilis (Brady), Calanopia elliptica (Dana) (both male and female), Temora turbinata (Dana), and Paracalanus aculeatus Giesbrecht (only female) from tropical inshore waters have been studied. Newly hatched Artemia nauplii (for Eucalanus, Tortanus, and Calanopia), Dunaliella (for Temora), and Skeletonema (for Paracalanus) were used as food. Feeding rates were measured for a single individual through successive incubations once or twice a day until death to determine changes in feeding rate after collection. Copepods survived from a few days to three weeks. In general, feeding rates varied from day to day, but were less variable than the differences between day and night rates. In some cases, feeding rate consistently decreased up to the death of the copepod. Daily ration, estimated in terms of percentage body weight, was in the range of 28–329 ‰ Using the results together with the those of other workers, gives the relation between daily ration (Y, % body weight) and body weight of copepods (X; μg dry weight) at 20 °C as, log Y = 2.531−0.377 log X. Copepods given Artemia nauplii as food killed more nauplii than were eaten. This phenomenon, tentatively called ‘over-hunting’, is possibly an important feeding behaviour for carnivorous copepods.

Relation of mosquito density to bird: mammal feeding ratios of Culex tarsalis in stable traps.

Stable traps, each baited with a jackrabbit and either a chicken or a pheasant, collected more than 21,000 mosquitoes in the Sacramento Valley, California, in 1972 and 1973. The focus of interest was the feeding behavior of Culex tarsalis, a primary vector of encephalitis viruses. Generally, feeding success was less and feeding rates on the jackrabbit were greater when larger numbers of mosquitoes were collected, or when a bird was exposed that was less receptive to mosquito feeding. Greater feeding rates on the jackrabbit apparently resulted from decreased feeding on the avian host and from diversion of mosquitoes to the jackrabbit. Figures are given that show how changes in feeding rates on birds affect the probabilities that a mosquito that feeds twice would feel both times on a bird, or on a bird and then on a mammal. Relatively small collections of nine mosquito species other than C. tarsalis revealed distinct species differences in feeding behavior. Aedes malanimon showed a preference for jackrabbit, which is relevant to its role as a vector of western equine encephalitis and California encephalitis viruses.

Reproductive cycles in oregon populations of the echlnoid, Strongylocentrotvs purpuratus (Stimpson). I. Annual gonad growth and ovarian gametogenic cycles

Four annual reproductive cycles were followed in the echinoid, Strongylocentrotus purpuratus (Stimpson), at three places on the central Oregon coast near 44°45′N lat., where intermittent upwelling depresses coastal sea temperatures from June through September. Monthly measurements were made of the gonad index of samples of 30 urchins and the relative frequency of five stages in oogenesis were determined from sectioned ovaries from these samples. Individuals in these populations are synchronous in their annual cycle of gonad growth, oogenesis, and spawning, the latter taking place between late December and March. The population usually undergoes one major, complete spawning within a period of 30 days. When large reserves of stored nutrients are present, ova continue to mature over a longer period and may be present in quantity from December into April. Gonad weight does not change significantly from March through June. From July through November the gonad undergoes its annual growth at a mean instantaneous relative growth rate of ≈ 1 % per day. Gonad growth is not significantly correlated with sea temperature. Variable temperatures resulting from upwelling do not result in erratic fluctuations in the reproductive cycle, probably because of the annual change in feeding rate, the seasonal shift in energy utilization, and the constancy of the amount of food assimilated during gonad growth. Gonad size and annual growth rates may differ significantly between years and locations, indicating that both are influenced by local environmental factors, probably food availability and degree of wave action. The frequency of oogonial clusters is least in mid-winter, increases after spawning, reaches an annual maximum in June and declines in the fall. Primary oocyte growth is very slow until October, when it increases abruptly, and some oocytes become ova as early as late October. When stored nutrients are low, many oocytes do not complete growth by January, and are not spawned until May. Prolongation of the spawning period delays the increase in frequency of oogonial clusters in the following new cycle. The timing of the annual increase in oogonial cluster frequency and of the onset of rapid oocyte growth did not otherwise vary between places and years. In these populations, entrainment or synchronization of the reproductive cycle to seasonal environmental events probably occurs at the beginning of one or all of these critical annual events: oogonial proliferation, annual gonad growth and rapid oocyte growth.