Reproductive Ecology Research Articles

Reproductive ecology of the prickly pear Opuntia atropes, a native plant subject to management

Reproductive ecology of the prickly pear Opuntia atropes, a native plant subject to management

Reproductive ecology of the Argus brief squid Lolliguncula argus in the coast off Oaxaca, southern Mexican Pacific

Abstract Lolliguncula argus is a squid species endemic to the Tropical Eastern Pacific and caught incidentally by the artisanal fishery around Puerto Angel, Oaxaca (Mexico). Due to the low abundance of Argus brief squid, basic aspects of the species’ reproductive biology have not been adequately studied. Therefore, in this study, we assess size at maturity (L50), gonad maturation, ovarian development and spawning pattern by means of both histological and oocyte size–frequency analyses. Our results are based on 581 squid specimens: 534 females (11.9–82.4 mm dorsal mantle length, DML) and 47 males (16.0–68.2 mm DML) caught by artisanal fishery from May 2017 to April 2018. The L50 was 58.0 mm DML for females and 55.4 mm DML for males. The ovulation pattern in L. argus is asynchronous, with multiple-batch spawning in a relatively short period of time (intermittent spawning). Lolliguncula argus breed in the coastal waters off Puerto Angel, in the western margin of the Gulf of Tehuantepec, and exhibit gregarious behaviour during spawning events, which is associated with the regional oceanographic conditions. Based on these results, we determine that the opportunistic reproductive strategy of L. argus occurs in response to suitable regional environmental conditions.

Bridging conservation across the ex situ-in situ spectrum: Insights into the reproductive ecology of the threatened narrow-headed gartersnake (Thamnophis rufipunctatus).

Zoo-based (ex situ) conservation breeding programs provide invaluable opportunities to uncover enigmatic behaviors and traits of focal species under managed care, which can support research and conservation management efforts. A suite of factors and a limited range have yielded population declines in the threatened narrow-headed gartersnake (Thamnophis rufipunctatus). Better understanding its cryptic ecology and life history (e.g., reproductive ecology) offers conservation benefits. We analyzed data on courtship behavior, parity and litter size, offspring size, and neonatal growth from an ex situ T. rufipunctatus population at the Phoenix Zoo from 2009 to 2018. Courtship behavior and parturition phenology are likely linked with the North American monsoon season, yet the courtship window may be wider than realized. We document the first instances of interannual iteroparity and multigenerational rearing of successful breeders at the ex situ level. Litter sizes varied but were relative to maternal body mass, suggesting that fecundity may be driven by intrinsic condition (e.g., age and size) of breeding females. Mean offspring body masses were equivalent between sexes, and neonate growth trends were quadratic during their first 9 months. Sexual dimorphism became apparent around 4-5 months age. Much of these data are novel for T. rufipunctatus and provide insight into their reproductive ecology. Phenology of reproductive ecology and body size metrics can guide field surveillance, age estimations, and population ecology monitoring, as well as inform ex situ adaptive management practices. Strategies spanning the ex situ-in situ spectrum are applicable to other imperiled taxa to better inform conservation management decisions.

Temporal distribution, reproductive synchrony, and mating patterns of the explosive breeder frog Dermatonotus muelleri (Anura: Microhylidae)

The knowledge about natural history of a species is fundamental for the proposition of theories in population, community, and behavioral ecology. Dermatonotus muelleri (Boettger, 1885) is one of the several Neotropical anuran species that still lacks basic information. These frogs are widely distributed in South America and present many peculiar morphological features, such as a reduced head size and a tongue morphology that suggests a specialized diet in ants and termites. However, D. muelleri is rare in anuran surveys, because of the explosive breeding behavior, which restrict its occurrence in aquatic habitats to few days a year, and the semi-fossorial habit, making the individuals inactive during most part of the year. In this study, we describe the reproductive ecology of Dermatonotus muelleri, with special attention to the mechanisms that regulates (i) the reproductive synchrony between males and females and (ii) the operational sex ratio (OSR), and (iii) if size is a good predictor of pairs formation (assortative mating).

The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization.

In an era of climate change, impacts on the marine environment include warming and ocean acidification. These effects can be amplified in shallow coastal regions where conditions often fluctuate widely. This type of environmental variation is potentially important for many nearshore species that are broadcast spawners, releasing eggs and sperm into the water column for fertilization. We conducted two experiments to investigate: 1) the impact of water temperature on sperm swimming characteristics and fertilization rate in sand dollars (Dendraster excentricus; temperatures 8-38°C) and sea urchins (Mesocentrotus franciscanus; temperatures 8-28°C) and; 2) the combined effects of multiple stressors (water temperature and pH) on these traits in sand dollars. We quantify thermal performance curves showing that sand dollar fertilization rates, sperm swimming velocities, and sperm motility display remarkably wide thermal breadths relative to red urchins, perhaps reflecting the wider range of water temperatures experienced by sand dollars at our field sites. For sand dollars, both temperature (8, 16, 24°C) and pH (7.1, 7.5, 7.9) affected fertilization but only temperature influenced sperm swimming velocity and motility. Although sperm velocities and fertilization were positively correlated, our fertilization kinetics model dramatically overestimated measured rates and this discrepancy was most pronounced under extreme temperature and pH conditions. Our results suggest that environmental stressors like temperature and pH likely impair aspects of the reproductive process beyond simple sperm swimming behavior.

Reproductive Ecology and Nesting Site Characteristics of Four-Toed Salamanders (Hemidactylium scutatum) in Natural and Constructed Upland-Embedded Wetlands on the Appalachian Plateau, Kentucky

Many forested freshwater wetlands have been altered or destroyed, and wetlands are constructed to offset loss. However, they do not always replace the function of natural wetlands. It is important to understand how features of the habitat differ between types of wetlands and whether constructed wetlands provide an adequate habitat for species adapted to natural wetlands. Our objectives were to measure the characteristics of Four-toed Salamanders’ nesting habitat and determine which factors contribute to the abundance of eggs and nests in natural and constructed upland-embedded wetlands within a ridgetop ecosystem in eastern Kentucky. We located and examined characteristics for 207 nests in twelve wetlands and measured variables at the nest level and at the wetland level. The best predictor of the number of eggs and number of nests was amount of moss at the wetland. These measures of reproductive effort were similar between types of wetlands, but the number of eggs per nest was higher in constructed wetlands and inversely related to amount of moss, highlighting a deficit in nesting habitat. Research of embryonic and larval survival is needed but based on data from other amphibian species in this system, we predict that the survival of Four-toed Salamanders’ larvae is low in constructed wetlands with permanent hydrology. Restoration of constructed wetlands should address the need for moss as nesting substrate and drying of the wetland to reduce the abundance and diversity of predators of larvae.

Comparative ecology of chasmogamous and cleistogamous reproduction inDanthonia compressa: effects of floral type and maternal environment

The significance of maternal and progeny environment to chasmogamy (CH) and cleistogamy (CL) in perennial plants is not well known. The perennial grass Danthonia compressa produces CH spikelets capable of outcrossing on terminal panicles in summer followed by selfing axillary CL spikelets in autumn. This study compared CH and CL seed mass, germination, seedling size, tillering, and reproduction in a sunny woodland edge and shaded interior habitat in the Catskill Mountains of New York State. CL seeds were significantly heavier than CH seeds. Numbers and mass of both seed types were greater in the edge. CL seeds showed much greater germination than CH seeds in both environments during spring, 2018; CL seedlings were larger than CH seedlings in the sunnier habitat. Survival was much greater in the edge than interior and higher for CL seedlings. After 27 months, maternal effects were mostly not detected and there was no significant effect of plant type (CH vs CL) on tiller production, final biomass, or reproduction via CH and CL. For this native grass, non-dispersed CL seeds may be more critical to seedling establishment and population persistence due to greater mass and germinability, and better plant survival, relative to smaller, dispersible CH seeds.

Variability in mating strategies in a widespread cactus in the Chihuahuan Desert

Opuntia is the most diverse and widespread genus in the Cactaceae; several species have broad distribution ranges and have successfully adapted to distinct habitats. One explanation for their success is the diversity of their reproductive systems. Opuntia macrocentra is one of the most common widespread species in North American deserts. A previous work on a northern population documented that this species has a mixed‐mating system and receives a low frequency of pollinators. In a southern population of O. macrocentra, we described its floral visitors, anthesis schedules and flower morphometry. Through controlled pollination experiments (selfing, outcrossing, supplementary pollen and natural pollination), we assessed the breeding and mating systems and measured pollen limitation. Eight different bee species visited the flowers. Based on their conduct, Diadasia rinconis and Lasioglossum sp. were the main pollinators. Flowers were homogamous and herkogamous. Floral traits and pollination experiments showed that O. macrocentra is xenogamous and self‐incompatible. Fruit set of the natural pollination, outcrossing and supplementary pollen treatments were not statistically different. Seed set was higher in natural pollination and the pollen limitation index for seed set was negative. Based on these results, we conclude that O. macrocentra is not pollen limited in the studied population. These results contrast with those of the previously studied population; therefore, we caution about making generalizations about the reproductive system based solely on studies in one population. The diversity of mating systems displayed by O. macrocentra may explain its broad distribution and adaptation to different environmental factors, one of which may be pollinator availability. Our results highlight the need to describe the reproductive ecology of populations instead of species, because reproductive systems and ecological factors such as plant–animal interactions may differ across their distribution range.

Is recruitment of brown trout in a New Zealand river driven by parental spawning investment, density dependence, or environmental factors?

This study addresses the primary factors driving young-of-the-year (YoY) brown trout Salmo trutta abundance and population dynamics through the Austral summer in an important spawning tributary of a large New Zealand river. We measured the key traits and spawning investment of spawners; YoY density and movement; and environmental characteristics important for juvenile trout. In comparison to their native European range, we found high rates of pre-spawning mortality, low density of deposited eggs and reduced spawning efficiency of adult brown trout. Parental spawning investment did not affect spring juvenile trout distribution, a result likely related to a mismatch between YoY abundance and densities of eggs deposited by adults at the sampled locations. Spatial differences in seasonal dynamics of YoY density were likely related to the diversity of environmental conditions affecting habitat suitability for post-larval brown trout along the stream. Significant correlations between juvenile trout loss rate and both YoY density and downstream migration were observed only for the lowland stream segments, which had the highest spawning investment from diadromous adults, indicating the importance of these locations for recruitment. This study highlights knowledge gaps in species-environment interactions and the reproductive ecology of brown trout in New Zealand.

Detecting denning behavior with camera traps: an example with fishers

Camera traps are often used to monitor wildlife occupancy and, increasingly, to record life history events. For tree-denning species such as fishers (Pekania pennanti), camera traps have been used to investigate reproduction (e.g., litter size and kit survival) by documenting females with kits as they move between trees. Yet, unbiased quantification of litter size and kit survival likely requires consideration of detection probability during transitions. We conducted a field experiment with the objective of estimating detection probability of fishers coming to or going from a central tree given different camera arrays and compared that to observations of collared females denning in northern New York. We estimated detection probability via logistic regression and investigated the effects of movement differences related to leaving vs. returning to the tree, as well as temporal effects related to kit development. The number of cameras deployed strongly influenced detection probability, which on average ranged from 0.21 with one camera to 0.85 with 6 cameras, yet detection rate of fishers returning to the den was consistently higher than fishers leaving. Despite the difference in detection relative to direction, we obtained at least one photo of 94% of expected kit transfers. Our results demonstrate the benefits and challenges of purpose-specific tests when using camera traps for estimating demographic rates, and we offer considerations for researchers that may be considering trade-offs between number of cameras and different collar technology in understanding reproductive ecology of fishers and similar arboreal-denning carnivores.

Reproductive Cycle and Sexual Group Maturity of Buccinum osagawai (Neogastropoda: Buccinidae)

This study was performed to obtain information on the basic reproductive ecology and biological resource management of Buccinum osagawai. Samples were collected from August 2018 to October 2019 with a drum-shaped net at a depth of 150–250 m along the continental shelf in Jumunjin, on the east coast of Korea. The species showed gonochorism and a lack of external sexual dimorphism. The overall sex ratio (F:M) was 1:1.2 (n = 549, F = 250, M = 299); as the size of the individuals increased, the proportion of males tended to decrease. The development pattern of the oocyte was synchronous, in which a dominant group of oocytes was identified within the same ovary. The size of the ripe oocyte was 82.3 (±22.6) × 125.5 (±22.0) μm. The spermatocyte development pattern was group-synchronous, in which multiple stages of germ cell populations were simultaneously identified within the same spermatogenic acinus. The gonad index (GI) for both males and females showed the highest value during June, after which it decreased sharply, and after August it was below 2.0. The main spawning season was from June to July, and the GI and stages of gonadal development did not show a pattern of seasonal changes. The main gonadal active season was from May to July, and both male and female gonadal development and maturation took place over a short period, whereas the recovery period after spawning was longer. At least 60.5% of the group, considering both males and females, showed maturity at 50.1 mm SH or more. Furthermore, the size of 50% group maturity was shown at approximately 50.0 mm SH.

Male genital organs of the black-crowned dwarf marmoset (Callibella humilis).

This study provides the first morphological description of the male genital organs of black-crowned dwarf marmoset (Callibella humilis). Internal and external genital organs were similar to other species of non-human primates. However, some shape and size differences were noted. The penile shaft was laterally flattened and comprised of two corpus cavernosus. These were split by a septum up to the level of the glans and then merged to form a single structure. The glans penis had small, keratinized spicules arising from epidermal or dermal projections. The small, fully ossified and well-mineralized penile bone, located at the distal end of the penis, consisted of a bone matrix surrounded by sparse osteoblasts and well-developed internal osteocytes. The penile urethra was lined with columnar pseudostratified epithelium, with areas of simple cuboidal epithelium. The testes were small relative to the body compared to other primate species. The findings of this work may support comparative studies of primate reproductive ecology.

Echinoderm fisheries: their culture, conservation, bioactive compounds and therapeutic applications

The Indo-Pacific region sometimes referred to as the Indo-West Pacific, is considered to be the richest marine biodiversity hotspot comprising unique species of echinoderms, molluscs, shrimps, crabs and fishes. These bioresources provide excellent opportunities for the studies of breeding biology, reproductive ecology, aquaculture, conservation, population genetics as well as species and speciation mechanisms of many diverged taxa. However, this interesting area is quite new and yet to be fully explored and determined. In the bottom-dwelling sessile invertebrates, echinoderms belonging to the phylum Echinodermata, have been considered the high-valued marine bioresource, having profound biological, aquacultural, conservational, nutritional and pharmaceutical significance. Among them, the sea urchins and sea cucumbers are both commercially fished and heavily overexploited. In sea urchins, the harvested product is the gonad, commonly known as "Sea urchin Roe”, which has been long traditions of consuming as a high delicacy food in Asian, Mediterranean and Western Hemisphere countries, and have long been used as a luxury food in Japan. The population of the Asian Pacific Region has been using it for a long time as a remedy for improving general living tone and treatment for a number of diseases. In the sea cucumber, the principal product is the boiled and dried body-wall or ‘bêche-de-mer’ for which there is an increasing demand in many tropical and subtropical countries. Sea cucumbers are also believed to exert wound healing and reduce arthritis pain in humans, hence are widely used in Asian folk medicine. However, due to a lack of proper management and conservation strategy in place, many sea urchin and sea cucumber fisheries are under threat. For this, cultivation of these species increasingly becomes a necessity, both for stock enhancement programs and as a means to meet the increasing market demand. Procedures for mass production of the tropical Holothuria scabra are now well established in China, India, Australia, Indonesia, the Maldives, the Solomon Islands, Philippines and Thailand. Alike many other marine organisms, echinoderms have been, and continue to be, examined as a source of biologically active compounds with biomedical applications. Most recently, a number of important bioactive compounds have been isolated from sea cucumbers and sea urchins, having distinctive biological and pharmacological activities including anti-angiogenic, anticancer, anticoagulant, anti-hypertension, anti-inflammatory, antimicrobial, antioxidant, antithrombotic, antitumor and wound healing activities. However, development patterns of echinoderm fisheries are largely expectable, often unsustainable and frequently too rapid for effective management. Proper steps should be undertaken on the potential ecosystem and human community consequences, appropriate aquaculture management strategies, and urge for better monitoring and reporting of catch and abundance, proper scientific research for stock enhancement and consideration of international biodiversity and trade regulations to ensure sustainable development and utilization of high-valued echinoderm fisheries to a greater extent.

Effects of habitat disturbance on the reproductive ecology of Arum pictum ssp. sagittifolium: from pollination to seedling recruitment.

The loss of natural habitats may strongly affect the fitness of plants that depend on animals for reproduction. However, very little is known regarding the differential effects of habitat disturbance on the distinct phases of the reproductive cycle of plants, especially in non-rewarding species. We assessed the effects of habitat disturbance on the entire reproductive cycle of Arum pictum ssp. sagittifolium, a species with deceptive pollination that is endemic to the western Mediterranean Basin. For this, we performed hand-pollination and bagging experiments, evaluated the role of pollinators and dispersers on reproduction, and estimated seedling recruitment in three natural and three disturbed populations (according to their surrounding natural habitat) in Mallorca Island. Pollinators were sphaerocerid flies (mainly Coproica, with ~50 % of visits) and staphylinid beetles, and were required for sexual reproduction. Habitat disturbance differently affected the reproductive phases of A. pictum ssp. sagittifolium. Habitat disturbance had a positive effect on Shannon pollinator diversity (but not on pollinator richness), and total pollinator and Coproica abundance were three times higher in disturbed habitats, where overall seed production was also ~30 % higher in natural habitats. Seed production increased with Coproica abundance, but only in natural habitats. Seed dispersers of A. pictum ssp. sagittifolium were birds, mainly Sylvia atricapilla. Although habitat disturbance did not influence disperser diversity or abundance, the majority of seedlings appeared under adult plants and in natural habitats. Overall recruitment was higher in natural habitats, but this effect could have been masked by only assessing pollinator and disperser numbers, as processes related to the quality of these interactions might be influencing fitness. Our study highlights the need to study different reproductive phases and their multiple components and processes to properly understand the effects of habitat disturbance on the regeneration of plant populations.

Nest‐boxes alter the reproductive ecology of urban cavity‐nesters in a species‐dependent way

Human‐provided nesting shelters such as nest‐boxes mitigate the shortage of natural breeding sites. Since artificial nests are not where animals evolved and optimised their reproductive performance, it remains inconclusive if these are adequate substitutes, ensuring equivalent fitness returns while breeding. In particular, most knowledge on the ecology of cavity‐nesting birds comes from nest‐box populations, but no study has directly compared fitness consequences of breeding inside nest‐boxes in relation to natural cavities in cities. We directly compare the reproductive performance, life‐history trait variation and fitness consequences for two small passerines, blue and great tits, breeding in nest‐boxes as opposed to natural cavities in an urban deciduous forest. We use a quasi‐experimental setting to comprehend the conservation potential of these artificial cavities and to support/question generalisations stemming from nest‐box studies. We show that the effects of cavity type vary between species: in blue tits, fitness proxies were negatively affected by nest‐boxes (lower fledging success and fledgling numbers, longer time spent in the nest and later fledging date relative to natural cavities), while in great tits, the fitness proxies were unaffected by cavity type. Importantly, we detected accelerated incubation in both species breeding in nest‐boxes. No differences in pre‐hatching traits (lay date, clutch size, hatching rates) between cavity types suggest that the fitness deterioration occurred because of post‐hatching effects. We highlight the ecological importance of old‐growth tree stands, providing natural cavities for city‐breeding animals and the need for quantifying alterations of reproductive ecology in other taxa using human‐provided nests. Owing to the detected cavity type‐dependent variation in reproductive performance, we support the criticism regarding the unconditional extrapolation of evolutionary and ecological interpretations of nest‐box studies to general populations.

Neglected plant parasites: Mitrastemonaceae

Mitrastemonaceae are a remarkable family of parasitic flowering plants. The two species that make up this family have a disjunct distribution and a peculiar appearance. Both are devoid of roots, stems, and regular leaves and live inside the roots of their host plants for most of their life cycle. Their white-pink flowers and berry-like fruits become visible on the forest floor only during their reproductive phase. This cryptic growth form, allied to their patchy distribution, and the muted color of their flowers have contributed to making Mitrastemonaceae one of the least collected and analyzed families of parasitic plants. On the other hand, recent findings regarding the phylogenetic position of the family have advanced our understanding of the family's biogeography and prompted a reexamination of their ecology and evolution. Here we review key aspects of the life cycle, reproductive ecology, and host relationships in the family Mitrastemonaceae to identify gaps in our current knowledge and instigate future research.

Reproductive ecology of Adelphobates quinquevittatus (Steindachner, 1864) in the southwestern Brazilian Amazon (Anura, Dendrobatidae)

Reproductive ecology of Adelphobates quinquevittatus (Steindachner, 1864) in the southwestern Brazilian Amazon (Anura, Dendrobatidae)

Factors influencing black spruce reproductive potential in the northern boreal forest of Quebec

The reproductive ecology of the semi-serotinous species black spruce ( Picea mariana (Mill.) BSP) in northern boreal forests remains poorly understood. There is a general lack of data on cone/seed production and viability as a function of biotic tree-level characteristics and abiotic variables. No studies currently exist to quantify these differences over a large gradient in temperature, elevation, and precipitation. Extensive physical, ecological, dendrometric, and reproductive data were collected from young to very old black spruce stands in northern Quebec. ANOVA and general linear mixed models were used to examine interannual cone production, and the relative importance of the biotic and abiotic explanatory factors in determining total cone production; length of the cone-bearing zone; filled seeds per cone; proportion of filled seeds; and seed viability. The results illustrate that the reproductive ecology of black spruce in northern cold forests is mainly explained by biotic variables such as age and diameter at breast height, and by abiotic variables related to temperature such as elevation, length of the growing season, and growing degree-days. Black spruce exhibits a lower reproductive potential in northern cold forests, making it possibly less resilient to increased fire frequency, particularly in unproductive and very young or very old stands.

Comparative reproductive ecology of two sister Asarum species (Aristolochiaceae) in relation to the evolution of elongated floral appendage.

Genus Asarum (Aristolochiaceae) shows diverse floral morphology and is hypothesized to have diversified as a result of pollinator-mediated selection. Yet most aspects of their reproductive ecology, including pollinators, remain unclear. This study focuses on A. costatum and A. minamitanianum in Japan, a sister species pair having remarkable differences in calyx lobe length (10-20 mm and 70-180 mm, respectively). The objectives of this study are to elucidate multiple aspects of reproductive ecology of these two species and obtain evolutionary insights into floral organ elongation. We adopted combined approaches, including field observations, molecular analyses and cultivation experiments, such as pollinator observation for 3 years, fine-scale spatial genetic analysis of 769 individuals, paternity analysis based on 566 seeds over 4 years, and control pollination experiments. Both Asarum species had strong spatial genetic structures, indicating limited seed dispersal. Pollinator observation revealed that flies and ground-dwelling insects visited flowers of both species, but that the pollinator fauna differed between the species. The visitation rate of flies was extremely low but was more than twice as high in the species with an elongated floral appendage. Paternity analysis revealed A. minamitanianum was predominantly outcrossing, while A. costatum showed a wide range of selfing rates among fruits. These two Asarum species are likely adapted to fly pollination in the shady forest understorey, where available pollinator fauna is limited. In addition, although its function remains unclear, the elongated calyx lobe of A. minamitanianum could have evolved for effective pollen dispersal by attracting fly visitors.

Reproductive Dynamics of an Isolated Population of American Crocodiles (Crocodylus acutus) Based on Long-term Monitoring Data

The American Crocodile (Crocodylus acutus) is still considered Vulnerable, with some populations remaining depressed and showing little evidence of recovery. An understanding of the reproductive dynamics and parameters of C. acutus is essential for its conservation and management. Although the knowledge of C. acutus reproductive ecology has greatly increased during recent years, some critical parameters such as breeding effort (i.e., proportion of adult females that nest each year in a population) remain poorly known. Herein we analyzed 14 yr of reproductive data from a C. acutus population in a Mexican atoll to better understand its reproductive dynamics in space and time. We estimated the number of reproductive females in the population and in each nesting area, compared nest characteristics and clutch parameters among nesting areas, and determined female breeding effort and breeding frequency (i.e., proportion of years that an adult female nested). We estimated that 35 reproductive female C. acutus inhabit the main island of the atoll, distributed among 12 nesting areas. The annual female breeding effort ranged from 27.3–60.6% and the breeding frequency of 15 selected females ranged from 57.1–92.3%. Breeding effort depends on the breeding effort in preceding years. We also found significant differences in reproductive attributes (i.e., number of nests, nest–water distance, nest depth, clutch size, and nesting success) among nesting areas that we explain by the quality of those habitats for crocodile nesting and by territorial behavior of females.