SEASONAL REPRODUCTION IN THE MALE AND FEMALE SPINY MOUSE (ACOMYS SPINOSISSIMUS) FROM SOUTH AFRICA

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CHAPTER 2 SEASONAL REPRODUCTION IN MALE AND FEMALE EASTERN ROCK ELEPHANT-SHREWS (ELEPHANTULUS MYURUS) FROM SOUTH AFRICA

Abstract

Environmental conditions vary throughout the year in most regions and, therefore, many small mammals reproduce at a specific time of the year to maximize reproductive success. In the tropics and sub-tropics, the breeding season is usually determined by the extent of the dry and rainy season and in many species, it was found that rainfall combined with the increase in food quantity and quality determines seasonal reproduction. We investigated the seasonality of reproduction in male and female Eastern rock elephant-shrews (Elephantulus myurus) from South Africa over a 12-months period by histological examination of the gonads and by measuring plasma testosterone and progesterone concentrations. In addition, animals were categorized into six relative age classes using the degree of maxillary molar tooth-row eruption and wear. Pregnant females were collected from August through to January and ovary size and plasma progesterone started to increase from July to August, peaked in October and regressed progressively thereafter. Follicular growth corresponded to this seasonal pattern of reproduction and Graafian follicles as well as corpora hemorrhagica, corpora lutea and corpora albicans were found from August until January, but not in the remaining months. Testes mass and volume, seminiferous tubule diameter and plasma testosterone concentration increased significantly from May and were highest from August until October after which they decreased. The distribution of relative age classes throughout the year confirmed that E. myurus is a seasonal breeder. In conclusion, E. myurus breeds seasonally during the warm and wet spring and summer months and stops breeding during the cold and dry winter months of the southern hemisphere. We suggest that seasonal reproduction evolved in E. myurus because of the severe seasonal changes in rainfall and ultimately food availability.
Keywords: Macroscelidea, follicular growth, food availability, rainy season, relative age, southern hemisphere

Introduction

Reproduction is costly (Partridge & Harvey, 1985) and, therefore, most mammals breed only during a specific time of the year when environmental conditions are favourable. However, many small mammals are opportunistic and may breed during harsh conditions as long as prolonged or year-round breeding offsets the costs and ultimately maximizes reproductive success (Beer & MacLeod, 1961; Scheffer, 1924). In the tropics, many mammals breed throughout the year because environmental conditions are more stable than in temperate regions. Seasonal reproduction has, however, also been reported and often occurs in conjunction with seasonal variation in rainfall (Delany, 1971; Delany & Neal, 1969). For example, the multimammate mouse (Mastomys natalensis) was found to breed during the rainy season, but to cease breeding during the dry season in several countries throughout Africa such as Uganda, Tanzania, Swaziland and South Africa (Bronner et al., 1988; Delany & Neal, 1969; Leirs et al., 1996; Monadjem, 1998; Neal, 1977)
Many temperate species, particularly Peromyscus species (Trainor et al., 2006), hamsters (Hegstrom & Breedlove, 1999; Prendergast et al., 2001) and voles (Kerbeshian et al., 1994) have been traditionally used to unravel the mechanisms of seasonal reproduction. On the other hand, the reproductive strategies of many tropical and sub-tropical mammals are still largely unknown (Bronson, 2009) and although a number of African rodent species have been investigated, many other species have been largely ignored. In southern Africa, seasonal as well as aseasonal and opportunistic breeding has been reported in small mammals. For example, the Namaqua rock mouse (Micalaemys namaquensis) and the Tete veld rat (Aethomys ineptus) breed during the spring and summer months (Muteka et al., 2006b; Muteka et al., 2006c), whereas the four-striped field mouse (Rhabdomys pumilio) breeds year-round in environments with mild winters and seasonally under harsh conditions (Jackson & Bernard, 2006).
Many different factors have been attributed to influence and shape seasonal reproduction. Photoperiod, the seasonally changing day/night cycle, is the most reliable at latitudes above 30° and is, therefore, mostly utilized by small mammals from temperate regions as a cue to predict events distant in time (Bradshaw & Holzapfel, 2007), but also sub-tropical rodents have been found to be reproductively photoresponsive (Muteka et al., 2006a; Chapter 3). However, rainfall in conjunction with an increase in food quantity and quality appears to be the major factor which controls seasonal reproduction at sub-tropical and tropical latitudes especially in habitats with distinct wet and dry seasons (Taylor & Green, 1976; Tinney et al., 2001). Ambient temperature, although less investigated, has likewise been found to influence reproduction. In the Nile grass rat (Arvicanthis niloticus), low temperatures stimulate testicular activity, whereas breeding is inhibited by high temperatures (Sicard et al., 1993)
The members of the family Macroscelidea, the elephant-shrews or sengis, are unique among the small mammals of Africa and are endemic to this continent (Skinner & Chimimba, 2005). Most elephant-shrew species have been found to be monogamous (FitzGibbon, 1997; Rathbun & Rathbun, 2006; Ribble & Perrin, 2005; Schubert et al., 2009), give birth to precocial young and have distinct male and female reproductive systems (Tripp, 1971; van der Horst, 1951; van der Horst & Gillman, 1941a; Woodall, 1995). Seasonal as well as aseasonal reproduction has been reported in various species of elephant-shrews (Neal, 1995). The Eastern rock elephant-shrew (Elephantulus myurus) has been documented to breed seasonally (Stoch, 1954; van der Horst, 1946, 1954; Woodall & Skinner, 1989). However, these studies, although often extensive, have either not taken environmental factors into account, pooled data from different localities and months or have not investigated reproduction over an entire year which makes it difficult to interpret the reproductive patterns of this species. We, therefore, investigated the seasonality of reproduction of E. myurus on a finer scale and over an entire year and also measured environmental factors such as temperature and rainfall in its habitat. In doing so, the present study attempts a first understanding of the ecological significance and the evolution of seasonal reproduction in this elephant-shrew. We further aim to characterize environmental factors which may shape seasonal reproduction in E. myurus.
The habitat of E. myurus is characterized by seasonal rainfall with the rainy season in the spring and summer months and a severe dry period in autumn and winter. We hypothesized that E. myurus breeds seasonally during the warm and wet spring and summer months (September – February) and ceases breeding during the cold and dry months of the year (March – August) of the southern hemisphere when conditions are less advantageous for reproduction and reproductive success may be low.

Materials and Methods

General

The study was carried out at Goro Game Reserve in the Soutpansberg region of the Limpopo Province, South Africa (22°58’S, 22°57’S; 29°25’E, 29°24’E). The elephant-shrews were trapped with Sherman live traps (H. B. Sherman Traps, Inc. Tallahassee, Florida, U.S.A.) baited with a mixture of oats, peanut butter and fish and set overnight around the rocky outcrops of the reserve. Eastern rock elephant-shrews were captured at the end of every month from September 2007 until August 2008. With the exception of September when only four males and six females were collected and November when only three individuals of both sexes were collected, five males and five females were collected each month. Hence a total of 59 females and 57 males were captured over the entire study period. On the day of capture, all animals were weighed to the nearest 0.001 g using a digital balance (Scout Pro SPU123, Ohaus Corporation, Pine Brook, New Jersey, U.S.A.) and body mass (g) was subsequently rounded to 0.1 g for further analyses. During transport and in the laboratory, elephant-shrews were housed in polyurethane cages containing wood shavings and fed with Pronutro (high protein cereal; Pioneer Foods Ltd., Bokomo Foods, Cape Town, South Africa), canned dog food (Promeal Ltd., Dassenberg, South Africa) and grated apples or carrots. Fresh food and water were provided daily in open dishes. In addition, meal worms were fed, especially in cases where animals did not want to feed. Animals were collected under permit number: CPM-333-00002 from the CITES and Permit Management Office, Department of Environmental Affairs, Limpopo Province. This study was approved by the animal ethics committee of the University of Pretoria (ethics clearance number: EC028-07).
Monthly rainfall (mm) and ambient temperature (°C) were recorded throughout the study period. Rainfall data were provided by the Goro Game reserve and two iButton digital temperature data loggers (Maxim Integrated Products, Dallas Semiconductor, U.S.A.) were used to measure ambient temperature to the nearest 0.01 °C. The iButtons were placed near the ground and protected from direct sunlight and measurements were taken every two hours, from which the mean monthly ambient temperature was calculated.
All elephant-shrews were euthanized with an overdose of halothane after they were kept in the laboratory for one to three days. The gonads of both males and females were dissected out and blood was obtained by exsanguinations from the heart. The blood was centrifuged at 3000 rpm for 15 mins and the blood plasma was stored at -35 °C until hormone analysis. The entire female reproductive tract was removed and any embryos or placental scars in the uterine horns were recorded. Female bodies were also examined for milk in the mammary glands because swollen teats, as a sign for lactation, were difficult to observe. The gonads were fixed in Bouin’s fluid for approximately 20 hrs and then stored in 70 % ethanol. Skulls were prepared by boiling and subsequent removal of any tissue with tweezers and finally used to determine the relative age of an individual using the degree of maxillary molar tooth-wear and eruption (DeBlase & Martin, 2001) (see “Relative age classes” section below). All specimens will be deposited in the mammal reference collection at the Ditsong National Museum of Natural History, Pretoria, South Africa.

Histology

After the removal of fat and connecting tissue, fixed ovaries and testes were weighed to the nearest 0.0001 g using a high precision scale (Ohaus Corp. Pine Brook, N.Y., U.S.A.) and the length and width were measured (mm) using a pair of digital calipers (Sylvac Opto RS 232, Ultra Praezision Messzeuge GmbH, Germany). Gonadal length and width were used to calculate ovarian and testicular volume (mm³) by using the formula for the volume of an ellipsoid as follows: V = 4/3 ab² where a represents half the maximum length and b half the maximum width (Woodall & Skinner, 1989). The gonads were subjected to a series of histological preparations, including dehydration and embedding in wax. Subsequently, both testes and ovaries were cut into 7 µm-thick sections with a rotary microtome (820 Spencer, American Optical, Scientific Instrument Division, Buffalo, N.Y., U.S.A.); while only a few sections were cut from the testes, each ovary was cut in its entirety. Sections were mounted in consecutive order on microscope slides with gelatin and dried in an oven at 36 °C for approximately 48 hrs and thereafter stained with Ehrlich’s haemotoxylin and counter-stained with eosin (Drury & Wallington, 1967).

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Acknowledgements 
Declaration 
SUMMARY 
GENERAL INTRODUCTION 
CHAPTER 1 SEASONAL REPRODUCTION IN THE MALE AND FEMALE SPINY MOUSE (ACOMYS SPINOSISSIMUS) FROM SOUTH AFRICA
CHAPTER 2 SEASONAL REPRODUCTION IN MALE AND FEMALE EASTERN ROCK ELEPHANT-SHREWS (ELEPHANTULUS MYURUS) FROM SOUTH AFRICA
CHAPTER 3 REPRODUCTIVE PHOTORESPONSIVENESS IN MALE SPINY MICE (ACOMYS SPINOSISSIMUS) FROM SOUTH AFRICA
CHAPTER 4  REPRODUCTIVE RESPONSES TO PHOTOPERIOD IN MALE EASTERN ROCK ELEPHANT-SHREWS (ELEPHANTULUS MYURUS) FROM SOUTH AFRICA
CHAPTER 5 KISSPEPTIN-IMMUNOREACTIVITY IN MALES AND FEMALES OF THE SEASONALLY BREEDING SPINY MOUSE (ACOMYS SPINOSISSIMUS) FROM SOUTH AFRICA: EFFECTS OF SEX AND SEASON
CHAPTER 6  KISSPEPTIN-IMMUNOREACTIVITY IN MALES AND FEMALES OF THE SEASONALLY BREEDING EASTERN ROCK ELEPHANTSHREW (ELEPHANTULUS MYURUS) FROM SOUTH AFRICA: EFFECTS OF SEASON BUT NOT SEX
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